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1444Journal of Food Protection, Vol. 67, No. 7, 2004, Pages 1444–1450Copyright , International Association for Food ProtectionPrevalence of High-Risk Egg-Preparation Practices inRestaurants That Prepare Breakfast Egg Entrées:An EHS-Net StudyROBIN LEE,1* MARK E. BEATTY,2 APRIL K. BOGARD,3† MICHAEL-PETER ESKO,4 FREDERICK J. ANGULO,2CAROL SELMAN,1 AND EHS-NET WORKING GROUP11EnvironmentalHealth Services Branch, Division of Emergency and Environmental Health Services, National Center for Environmental Health,Centers for Disease Control and Prevention, 4770 Buford Highway N.E., Atlanta, Georgia 30341; 2Foodborne and Diarrheal Diseases Branch,Division of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, 1600 Clifton RoadN.E., Atlanta, Georgia 30333; 3Foodborne, Vectorborne and Zoonotic Diseases Unit, Infectious Disease Epidemiology, Prevention and Control,Minnesota Department of Health, 717 Delaware Street, Minneapolis, Minnesota 55414; and 4Environmental Health Specialists Network, CaliforniaEmerging Infections Program, 1212 Broadway, Oakland, California 94612, USAMS 03-529: Received 14 November 2003/Accepted 2 February 2004ABSTRACTSalmonella enterica serotype Enteritidis (SE) is a common cause of foodborne illness in the United States. Foods preparedwith raw shell eggs have often been associated with SE outbreaks. The federal government published the Egg Safety ActionPlan in December 1999 that called for reduction of egg-preparation practices that may contribute to the survival and prolif eration of SE. In seven states, an interview and brief site evaluation of 153 restaurants that prepare eggs during all hours ofoperation was conducted by the Environmental Health Specialists Network to determine the prevalence of such practices.Fifty-four percent (83 of 153) of restaurants pooled raw shell eggs not intended for immediate service. These pooled eggswere held a median of 4 h for scrambled eggs, 5.5 h for omelets, and 6 h for pancakes and French toast. Nearly 26% (39 of152) of restaurants reported storing eggs at room temperature, and 5% (7 of 152) stored eggs on ice or in cold-water bathsbefore cooking. Generally, eggs were cooked to 72 to 83 C, which is above the recommended final cook temperature of 63to 68 C. Employees reported sanitizing utensils used to prepare eggs less than once every 4 h in 42% (57 of 136) of restaurants.Several areas were identified in which further emphasis might reduce egg-associated SE infections in accordance with HealthyPeople 2010 goals.Infection with Salmonella enterica serotype Enteritidis(SE) remains an important public health problem in theUnited States. Although most foodborne illnesses go un reported, an estimated 1.4 million Salmonella infections oc cur each year in the United States (16). In 2001, 18% ofisolates in the National Salmonella Surveillance systemwere SE (4). Numerous studies, including investigations ofoutbreaks, indicate many of these infections are acquiredfrom eating SE-contaminated eggs (11, 19). In 2001, 23states reported 46 confirmed SE-associated outbreaks to theCenters for Disease Control and Prevention (CDC), result ing in 1,681 reported illnesses and 102 hospitalizations. Ofthe 46 outbreaks reported in 2001, 61% (28 outbreaks) oc curred in commercial food establishments. Implicated fooditems associated with transmission of the illness were con firmed in 52% (24) of the outbreaks, and eggs were iden tified 63% (15) of the time as an ingredient of the impli cated food item (5).* Author for correspondence. Present address: Health InvestigationsBranch, Division of Health Studies, Agency for Toxic Substances andDisease Registry, 1600 Clifton Road N.E., Atlanta, GA 30333, USA.Tel: 404-498-0605; Fax: 404-498-0079; E-mail: [email protected]† Present address: Princess Cruises, 24200 Magic Mountain Parkway,Santa Clarita, CA 91355, USA.In 1999, the President’s Council on Food Safety andconsumer and egg-industry advocates identified egg safetyas an area of concern warranting immediate federal inter agency action. This initiative led to the development of theCouncil’s Egg Safety Action Plan to reduce the number ofSE infections in the United States (20). Reducing the num ber of SE outbreaks is also one of the goals of the U.S.Department of Health and Human Services Healthy People2010 initiative (27).Because a substantial number of outbreaks have oc curred in restaurants (3, 5, 12, 19, 24), studies are specifi cally needed to determine the prevalence of high-risk eggpreparation practices in restaurant kitchens. High-risk foodpreparation practices associated with SE transmission in clude those that allow proliferation or survival of SE in oron eggs. Mixing of shelled raw eggs and then subsequentlystoring them at temperatures higher than the U.S. Food andDrug Administration (FDA) recommendation of 7 C (9)can permit one egg to contaminate a large batch of pooledeggs. The pooling of eggs has been documented as a foodpreparation practice that results in outbreaks of SE infection(26). Other practices that support SE proliferation includeimproper hot or cold holding of eggs (3, 15). SE can sur vive when eggs are not cooked properly (19). Hedberg etal. (11) demonstrated that eating soft or slightly under

J. Food Prot., Vol. 67, No. 7cooked scrambled eggs was associated with SE infection.Other high-risk food-preparation practices may facilitatecontamination of equipment, food worker hands, or fooditems with SE. Contamination of properly cooked eggs bycontact with contaminated items, such as improperlywashed hands, has also been associated with SE transmis sion (1, 12, 14). The risk for SE transmission can be mark edly reduced by use of pasteurized eggs, including pas teurized shell eggs, particularly in entrees containing un dercooked eggs (13, 25).The objective of this study was to identify the preva lence of high-risk egg-preparation practices and evaluaterestaurant egg-preparation policies, including the use ofpasteurized eggs, that may facilitate or hinder transmissionof SE in restaurants that prepare a large volume of eggproducts.MATERIALS AND METHODSThis study was conducted by staff of the EnvironmentalHealth Specialists Network (EHS-Net). The network, created bythe CDC comprises environmental health specialists and epide miologists at federal, state, and local levels who collaborate toevaluate food-preparation practices and policies and their relationto foodborne illness.The EHS-Net selected a convenience sample of restaurantsdefined as facilities that prepare and serve breakfast-type egg en trées to customers throughout all hours of operation in 13 met ropolitan areas in seven states: California, Connecticut, Colorado,Minnesota, New York, Oregon, and Tennessee. Each of thesestates participates in CDC’s Emerging Infections program. Res taurants that serve breakfast-type egg entrées throughout the entireday were selected because they use large quantities of shell eggsand therefore have a large potential for handling SE-infected eggs.Lists of restaurants that met this definition were not available inall states; therefore, restaurants were selected by the most com prehensive list of food-service establishments available to the lo cal regulatory authority. A database of restaurant ownership, num ber of meals served, or seating capacity was not available or easilyobtainable in each state; thus, stratifying selection on these param eters was not possible. Only one restaurant from regional or na tional chains was included per area.After obtaining permission from the restaurant, an EHS-Netspecialist or a trained local environmental health specialist con ducted an on-site interview with either the restaurant manager oranother employee using a standardized questionnaire. The ques tionnaire included both checklists and open-ended questions aboutthe restaurant demographics, food safety policies, and practicesrelated to the preparation of omelets, soft-boiled eggs, hard-boiledeggs, fried eggs, scrambled eggs, poached eggs, French toast, andpancakes. Demographic information included restaurant owner ship (independently owned versus a chain or franchise), whereeggs were purchased, and the type of eggs used in the facility.Data collected on food safety policies and sanitation included in formation about manager food safety certification requirements,storage of shell eggs, the use of pasteurized and nonpasteurizedshell eggs, type of egg entrées prepared, pooling of shelled eggs,and cooking practices. For this evaluation pooling of shelled eggsconsists of breaking and combining more than one shell egg inpreparation of multiple entrées not intended for immediate ser vice. Two open-ended questions were used to identify the locationof shell eggs before cooking and restaurant policy on washing andsanitizing whisks and bowls used to prepare egg entrées. Respons EGG-PREPARATION PRACTICES1445es to the questions about where shell eggs are kept before cookingwere classified into one of three categories: (i) eggs kept in acooling unit before cooking, (ii) eggs stored at room temperaturebefore cooking, and (iii) eggs kept on ice or in a cold-water bathbefore cooking. Responses to the question concerning restaurantpolicy on washing and sanitizing whisks and bowls used to pre pare egg entrées were categorized into three groups: (i) whisksand bowls washed and sanitized at least once in 4 h, (ii) whisksand bowls washed and sanitized once in a 4- to 24-h period, and(iii) responses that did not fall into either of the aforementionedcategories (e.g., utensils were washed and sanitized when needed,with no specific timeline noted). This study did not address theFDA Food Code recommendation 4-602.11, which stipulates thatutensils and equipment may be cleaned less frequently than every4 h if these items are kept in a refrigerated room or in an areamaintained at specified temperatures and that these items becleaned at a frequency specified based on the corresponding tem perature (9).Each interview was followed by a limited observational as sessment that involved measuring the internal temperature of oneuncooked shell egg in a cooling unit, taking final cook tempera tures of three egg entrées, and assessing the location of handwashing facilities. From the batch of stored shell egg in a coolingunit, one egg was selected from the most central location to de termine the internal temperature of an uncooked refrigerated shellegg. The temperature of the refrigerated shell egg was taken byinserting a thermocouple into the shell. Temperatures of an ome let, scrambled eggs, and French toast, prepared with no specialrequests, were measured using a thermocouple. Final cook tem peratures were taken immediately after the entrée was cooked andimmediately before it was served. All site visits were conductedat the restaurants 22 January through 26 February 2002.Data were entered into Epi Info 6.04d (7). Microsoft Excel2000 was used to categorize responses to open-ended questions(2). Data were analyzed using univariate and bivariate analysesperformed with SAS 8.2 for Windows 2000 (23). Prevalence oddsratios (PORs) were used to investigate trends and differences inspecific egg-preparation practices.RESULTSDemographics. A total of 153 restaurants were studied(Table 1). Of these, 63% (96 of 152) were independentlyowned restaurants, and 37% (56 of 152) were corporatechains or franchises. A median of 200 (25% quartile 130;75% quartile 450) meals were served per day. All 153restaurants used shell eggs. Eggs purchased were primarilygrade AA shell eggs (109 of 141) from a wholesaler (124of 153). Many restaurants used additional egg productssuch as pasteurized shell eggs (30 of 148), liquid egg prod ucts (88 of 153), and powdered egg product (9 of 150).Food safety policies. Seventy percent (99 of 141) ofrestaurants reported that at least one manager had receivedfood safety certification. Fifty-five percent (75 of 136) ofrestaurants reported washing and sanitizing their whisksand bowls at least once in 4 h. Nearly 42% (57 of 136)reported washing and sanitizing at least once during a 4- to24-h period, and 3% (4 of 136) of the responses fell intothe other category (Table 2).Egg-preparation practices. Twenty-six percent (39 of152) of restaurants reported holding eggs at room temper ature before cooking, and 5% (7 of 152) kept eggs on ice

1446LEE ET AL.J. Food Prot., Vol. 67, No. 7TABLE 1. Demographics for 153 restaurantsParameterRestaurant ownershipIndependentChain or franchiseMissingaEgg sourceWholesalerLocal producerOtherNo. (%) ofrestaurants96 (63)56 (37)1124 (81)27 (18)2 (1)Shell eggs usedYesNo153 (100)0Grade of shell eggsGrade AAGrade AMissinga109 (77)32 (23)12Pasteurized shell eggs usedYesNoMissinga30 (20)118 (80)5Liquid eggs usedYesNoPowdered eggs usedYesNoMissingaaTABLE 2. Self-reported egg-handling policies and practices in153 restaurantsPolicies and practicesNo. (%) ofrestaurantsManager(s) has food safety certificationYesNoMissinga99 (70)42 (30)12Restaurants pool shelled eggsYesNo83 (54)70 (46)Whisks and bowls washed and sanitizedAt least once in 4 h4–24 hOtherMissinga75 (55)57 (42)4 (3)17Shell eggs held before cookingIn a cooling deviceAt room temperatureOn ice or in cold-water bathMissingaa106 (70)39 (26)7 (4)1Information was not provided and therefore was not included inanalyses.88 (58)65 (42)9 (6)142 (94)2Information was not provided and therefore was not included inanalyses.or in a cold-water bath before cooking (Table 2). Twentypercent (30 of 148) of restaurants used pasteurized shelleggs; 2 of those 30 restaurants used pasteurized shell eggsto prepare each of the eight egg entrées surveyed. The per centages of egg entrées prepared with pasteurized shell eggsversus nonpasteurized shell eggs were similar for all eggentrées. Overall, restaurant chains and franchises used pas teurized shell eggs to prepare egg entrées significantly moreoften (POR 5; 95% confidence interval 2, 11) thandid independently owned restaurants (36% [20 of 56] ofrestaurant chains, 10% [10 of 96] of independent restau rants). Because of small sample size, this POR was notadjusted for modifiers such as volume of eggs prepared orthe number of breakfast entrees prepared with pasteurizedshell eggs.Ninety-five percent (146 of 153) of restaurants reportedpreparing fried eggs. Poached eggs were prepared by 86%(132 of 153) of restaurants. Among restaurants that madeomelets and scrambled eggs, 84% (128 of 153) used shelleggs to make omelets, and 86% (131 of 153) used shelleggs to prepare scrambled eggs. A median of two shell eggswere used to cook one order of pancakes, one order ofFrench toast, an omelet, or one order of scrambled eggs.Shelled eggs were pooled in 54% (82 of 153) of res-taurants: 69% (66 of 96) of independently owned restau rants and 29% (16 of 56) of chains and franchises. Poolingpractices were determined for the preparation of omelets,scrambled eggs, and the combined preparation of pancakesand French toast. The median number of shelled eggspooled was 18 (25% quartile 12; 75% quartile 30) forthe preparation of pancakes or French toast, 48 (25% quar tile 24; 75% quartile 90) for the preparation of om elets, and 36 (25% quartile 18; 75% quartile 90) forscrambled eggs. The median amount of time between thethe pooling of shelled eggs and the cooking of the productwas 4 h (25% quartile 2 h; 75% quartile 24 h) forscrambled eggs, 5.5 h (25% quartile 3 h; 75% quartile 24 h) for omelets, and 6 h (25% quartile 3.25 h; 75%quartile 24 h) for pancakes or French toast.Many restaurants in this study used nonpasteurizedshell eggs to prepare soft or runny egg entrées. Soft orrunny fried eggs were prepared by 78% (94 of 121) ofrestaurants, runny omelets by 42% (44 of 104), and softpoached eggs by 74% (83 of 112) (Table 3). Whether softor runny e

owned restaurants, and 37% (56 of 152) were corporate chains or franchises. A median of 200 (25% quartile 130; 75% quartile 450) meals were served per day. All 153 restaurants used shell eggs. Eggs purchased were primarily grade AA shell eggs (109 of 141) from a wholesaler (124 of 153). Many restaurants used additional egg products

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